A scorpion α-like toxin that is active on insects and mammals reveals an unexpected specificity and distribution of sodium channel subtypes in rat brain neurons

Journal of Neuroscience

Volumn 19, Issue 20, 1999, Pages 8730-8739

  Gilles, Nicolas ^a   Blanchet, Christophe ^b   Shichor, Iris ^c   Zaninetti, Marc ^b   Lotan, Llana ^c   Bertrand, Daniel ^b   Gordon, Dalia ^a,c  

^a CEA SACLAY   (France)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Chick central neurons; Expression in oocytes; Hippocampus slices; Insect sodium channels; Rat brain synaptosomes; Receptor site 3; Scorpion like toxin; Scorpion toxin; Sodium channel subtypes

Indexed keywords

RECEPTOR SUBTYPE; SCORPION VENOM; SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN NERVE CELL; BRAIN SYNAPTOSOME; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; TOXIN ANALYSIS;

EID: 0033570298     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-20-08730.1999     Document Type: Article

References (51)

1. + channel α subunit with novel gating properties. Neuron 1:449-461.
2. Beckh S (1990) Differential expression of sodium channel mRNA in rat peripheral nervous system and innervated tissues. FEBS Lett 262:317-322.
3. Beckh S, Noda M, Lubbert H, Numa, S (1989) Differential regulation of three sodium channel RNAs in the rat central nervous system during development. EMBO J 12:3611-3616.
4. Bertrand D, Bader CR (1986) DATAC: a multipurpose biological data analysis program based on a mathematical interpreter. Int J Biomed Comput 18:193-202.
5. Black JA, Yokoyama S, Higashida H, Ransom BR, Waxman SG (1994) Sodium channels mRNAs I, II and III in the CNS: cell-specific expression. Mol Brain Res 22:275-289.
6. Catterall WA (1992) Cellular and molecular biology of voltage-gated sodium channels. Physiol Rev 72:S15-S48.
7. Catterall WA, Beress L (1978) Sea anemone toxin and scorpion toxin share a common receptor site associated with the action potential sodium ionophore. J Biol Chem 253:7393-7396.
8. Cestèle S, Ben Khalifa R, Pelhate M, Rochat H, Gordon D (1995) α-Scorpion toxins binding on rat brain and insect sodium channels reveal divergent allosteric modulations by brevetoxin and veratridine. J Biol Chem 270:15153-15161.
9. Cestèle S, Stankiewicz M, Mansuelle P, Dargent B, De Waard M, Gilles N, Pelhate M, Rochat H, Martin-Eauclaire MF, Gordon D (1999) Scorpion α-like toxins, toxic to both mammals and insects, differentially interact with receptor site 3 on voltage-gated sodium channels in mammals and insects. Eur J Neurosci 11:975-985.
10. Chahine M, Plante E, Kallen RG (1996) Modulation of heart and skeletal muscle sodium channel α-subunits expression in tsA201 cells. J Membr Biol 152:39-48.
11. 50) of an enzymatic reaction. Biochem Pharmacol 22:3099-3108.
12. Dietrich PS, McGivern JG, Delgado SG, Koch BD, Eglen RM, Hunter JC, Sangameswaran L (1998) Functional analysis of a voltage-gated sodium channel and its splice variant from rat dorsal root ganglia. J Neurochem 70:2262-2272.
13. Dong K (1997) A single amino acid change in the Para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroach. Insect Biochem Mol Biol 27:93-100.
14. Eitan M, Fowler E, Herrmann R, Duval A, Pelhate M, Zlotkin E (1990) A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: purification, primary structure, and mode of action. Biochemistry 29:5941-5947.
15. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG (1997) Sodium channel α-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Mol Brain Res 45:71-82.
16. + current in Xenopus oocytes. J Neurosci 12:3743-3752.
17. Goldin AL (1995) Voltage gated sodium channels. In: Handbook of receptors and channels series, ligand- and vcltage-gated channels (Noth RA, ed), pp 73-111. Boca Raton, FL: CRC.
18. Gordon D (1997) Sodium channels as targets for neurotoxins: mode of action and interaction of neurotoxins with receptor sites on sodium channels. In: Toxins and signal transduction (Lazarowici P, Gutman Y, eds), pp 119-149. Amsterdam: Harwood.
19. Gordon D, Zlotkin E (1993) Binding of an α scorpion toxin to insect sodium channels is not dependent on membrane potential. FEBS Lett 315:125-129.
20. II sodium channel subtypes. Proc Natl Acad Sci USA 84:8682-8686.
21. Gordon D, Martin-Eauclaire MF, Cestclc S, Kopeyan C, Carlier E, Ben Khalifa R, Pelhate M, Rochat H (1996) Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J Biol Chem 271:8034-8045.
22. Gordon D, Savarin P, Gurevitz M, Zinn-Justin S (1998) Functional anatomy of scorpion toxins affecting sodium channels. J Toxicol Toxin Rev 17:131-158.
23. Gray EG, Whittaker VP (1962) The isolation of nerve ending from brain: an electron-microscopic study of cell fragments derived by homogcnization and centrifugation. J Anat 96:79-96.
24. Henderson CE, Bloch-Gallego E, Camu W (1995) Purified embryonic motoneurons. In: Nerve cell culture: a practical approach (Cohen J, Wilkin G, eds), pp 69-81. London: Oxford UP.
25. Jover E, Couraud F, Rochat H (1980) Two types of scorpion neurotoxins characterized by their binding to two seoarate receptor sites on rat brain synaptosomes. Biochem Biophys Res Commun 95:1607-1614.
26. Kanner BJ (1978) Active transport of γ-amino butyric acid by membrane vesicles isolated from rat brain. Biochemistry 17:1207-1211.
27. Kayano T, Noda M, Flockerzi V, Takahashi H, Numa S (1988) Primary structure of rat brain sodium channel III deduced from the cDNA sequence. FEBS Lett 288:187-194.
28. Kopeyan C, Mansuelle P, Martin-Eauclaire MF, Rochat H, Miranda F (1993) Characterization of toxin III of the scorpion Leiurus quinquestriatus quinquestriatus: a new type of α-toxin highly toxic both to mammals and insects. Nat Toxins 1:308-312.
29. Krimm I, Gilles N, Sautière P, Stankiewicz M, Pelhate M, Gordon D, Lancelin JM (1999) N MR Structures and Activity of a Novel α-Like Toxin from the Scorpion Leiurus quinquestriatus hebraeus. J Mol Biol 285:1749-1763.
30. + channel brings about short-term modulation by cAMP and β1-adrenergic receptor activation. J Mol Neurosci 7:269-276.
31. Little MJ, Zappia C, Gilles N, Connor M, Tyler MF, Martin-Eauclaire MF, Gordon D, Nicholson GM (1998) δ-Atracotoxins from Australian Funnel-Web Spiders compete with scorpion α-toxin binding but differentially modulate alkaloid toxin activation of voltage-gated sodium channels. J Biol Chem 273:27076-27083.
32. Loughney K, Kreber R, Ganetzky, B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143-1154.
33. Mandel G (1992) Tissue-specific expression of the voltage-sensitive sodium channel. J Membr Biol 125:193-205.
34. Martin-Eauclaire MF, Couraud F (1995) Scorpion neurotoxins: effects and mechanisms. In: Handbook of Neurotoxicology (Chang LW, Dyer RS, eds), pp 683-716. New York: Marcel Dckker.
35. Ray R, Morrow CS, Catterall WA (1978) Binding of scorpion toxin to receptor sites associated with voltage-sen iitive sodium channels in synaptic nerve ending particles. J Biol Chem 253:7307-7313.
36. Rogers JC, Ou Y, Tanada TN, Scheuer T, Catterall WA (1996) Molecular determinants of high affinity binding of α-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the sodium channel a subunit. J Biol Chem 271:15950-15962.
37. Sangameswaran L, Fish LM, Koch BD, Rabert DK, Delgado SG, Ilnicka M, Jakeman LB, Novakovic S, Wong K, Sze P, Tzoumaka E, Stewart GR, Herman RC, Chan H, Eglen RM, Hunter JC (1997) A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J Biol Chem 272:14805-14809.
38. Sarao R, Gupta SK, Auld VJ, Dunn RJ (1991) Developmentally regulated alternative RNA splicing of rat brair sodium channel mRNAs. Nucleic Acids Res 19:5673-5679.
39. Sautière P, Cestèle S, Kopeyan C, Martinage A, Drobecq H, Doljansky Y, Gordon D (1998) New toxins acting on sodium channels from the scorpion Leiurus quinquestriatus hebraeus suggest a clue to mammalian versus insect selectivity. Toxicon 36:1141-1154.
40. Schaller KL, Krzemien DM. Yarowsky PJ, Krueger BK, Caldwell JH (1995) A novel, abundant sodium channel expressed in neurons and glia. J Neurosci 15:3231-3242.
41. Shon KJ, Olivera BM, Watkins M, Jacobsen RB, Gray WR, Floresca CZ, Cruz LJ, Hillyard DR, Brink A, Terlau H, Yoshikami D (1998) μ-Conotoxin PIIIA, a new peptide for discriminating among Tetrodotoxin-sensitive Na channel subtypes. J Neurosci 18:4473-4481.
42. Stuhmer W, Conti F, Suzuki H, Wang X, Noda M, Yahagi N, Kubo H, Numa S (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339:597-603.
43. Thomsen WJ, Catterall WA (1989) Localization of the receptor site for α-scorpion toxins by antibody mapping Implications for sodium channel topology. Proc Natl Acad Sci USA 86:10161-10165.
44. Toledo-Aral JJ, Moss BL, He ZJ, Koszowski AG, Whisenand T, Levinson SR, Wolf JJ, Silos-Santiago I, Halegoua S, Mandel G (1997) Identification of PN1, a predominant voltage dependent sodium channel expressed principally in peripheral neurons. Proc Natl Acad Sci USA 94:1527-1532.
45. Vargas O, Martin MF, Rochat H (1987) Characterization of six toxins from the venom of the Moroccan scorpion Buthus occitanus mardochei. Eur J Biochem 162:589-599.
46. Vega-Saenz de Miera E, Rudy B, Sugimori M, Llinas R (1997) Molecular characterization of the sodium channel subunits in mammalian cerebellar Purkinje cells. Proc Nail Acad Sci USA 94:7059-7064.
47. Wallner M, Weigl L, Mcera P, Lotan I (1993) Modulation of the skeletal muscle sodium channel α-suhunit by the β,-subunit. FEES Lett 336:535-539.
48. Warmke JW, Reenan R, Wang P, Qian S, Arena J, Wang Wunderler DJ, Liu K, Kaczorowski G, Van der Ploeg L, Ganetzky B, Cohen C (1997) Functional expression of Drosophila para sodium channels modulation by the membrane protein TipE and toxin pharmacology. J Gen Physiol 110:119-133.
49. Weiland GA, Molinoff PB (1981) Quantitative analysis of drug-receptor interactions: I. Determination of kinetic and equilibrium properties. Life Sci 29:313-330.
50. + channel subtypes in central neurons. Neuron 3:695-704.
51. Zlotkin E, Miranda F, Rochat H (1978) Chemistry and pharmacology of Buthinae scorpion venoms. In: Arthropods venoms (Bettini S, ed), pp 317-369. New York: Springer.